Published online: 2020-01-10 THIEME Review Article 99

The Role of Interventional in the Management of Pancreatic Pathologies

Ghali Salahia1 Sook Cheng Chin2 Ian Zealley2 Richard D. White1

1Department of Radiology, University Hospital of Wales, Cardiff, Address for correspondence Ghali Salahia, MD, MBA, Department United Kingdom of Radiology, University Hospital of Wales, Heath Park Way, Cardiff, 2Department of Radiology, Ninewells Hospital, Dundee, United CF14 4XW, United Kingdom (e-mail: [email protected]). Kingdom

J Gastrointestinal Abdominal Radiol ISGAR 2020;3:99–114

Abstract Pancreatic pathologies are varied and wide-ranging, and a multidisciplinary approach is essential for effective diagnosis and management. We describe image-guided percutaneous (nonendoscopic) interventions in the management of pancreatic dis- ease, with emphasis on inflammatory and neoplastic pancreatic pathologies and on the transplanted . Image-guided treatments for the complications of pan- Keywords creatitis include percutaneous interventions on simple and complex peripancreatic ►►interventional collections, pseudocysts, and . Vascular interventions predominantly focus on radiology the ­treatment of pseudoaneurysms, hemorrhagic pseudocysts, and arteriovenous ►►pancreatic cancer malformations. Emerging ablative techniques for pancreatic cancer are promising ►►pancreatic transplant and include percutaneous radiofrequency ablation, microwave ablation, irreversible ►►pancreatitis electroporation, and electrochemotherapy. Image-guided interventions on the trans- ►►peripancreatic planted pancreas commonly include percutaneous biopsy and drainage in addition to

collection endovascular treatments of vascular complications.

Introduction offers diabetic patients the pros- pect of glycemic control free of exogenous insulin adminis- Approximately 20% of patients with acute pancreatitis will tration, with a significant improvement in quality of life and 1 develop complications that require intervention. These can reduction in diabetes-associated complications.6 Surgery 2 be classified into vascular and nonvascular complications : can, however, be complicated by a high rate of early techni- •• Nonvascular complications include collections, bowel cal failure.7 Percutaneous and endovascular interventions are complications, and pancreatic fistulas.2 increasingly performed for the diagnosis of rejection and the •• Vascular complications include peripancreatic arterial and treatment of vascular complications. venous pseudoaneurysms, venous thrombosis, and arte- 3 riovenous malformations (AVMs). Nonvascular Interventions Pancreatic adenocarcinoma is the 12th most common Drainage of Peripancreatic Collection malignancy and the 7th leading cause of cancer-related mor- Intra-abdominal collections and abscesses are the most com- tality globally.4 Most patients present late with either locally mon complication following acute pancreatitis.8 Collections extensive or metastatic disease.5 The aggressive nature, late are classified according to the revised Atlanta Classification presentation, and lack of effective therapies all contribute to into acute peripancreatic fluid collections, pseudocysts, the poor prognosis. Patients with more advanced disease will acute necrotic collections, and walled-off pancreatic necro- typically undergo either endoscopic ultrasound (US) or inter- sis9,10 (►Fig. 1). Symptomatic intra-abdominal collections ventional radiology-guided interventions to deliver either require imaging-guided drainage. When a collection is readily palliative or preoperative care.4

DOI https://doi.org/ ©2020 Indian Society of 10.1055/s-0039-3401335 Gastrointestinal and Abdominal ISSN 2581-9933. Radiology 100 Role of in the Management of Pancreatic Pathologies Salahia et al.

Fig. 1 (A) Acute peripancreatic fluid collection (green arrow). (B) Multiple pseudocysts (yellow arrows) in the context of acute on chronic pancreatitis (note the pancreatic calcifications). (C) Acute necrotic collection (note absent enhancement of the pancreatic head). (D) Percuta- neously drained walled-off necrosis (blue arrow indicate the wall). (E) This had been subsequently infected (note the presence of gas).

visualized on US, US-guided percutaneous drainage place- Infected pancreatic necrosis is often poorly marginated ment is generally the preferred choice as US is less expensive, and nonenhanced and may contain bubbles of gas. However, allows for real-time monitoring of the needle placement, and these features are not always present, and necrotic collec- is free from ionizing radiation.11 However, the combination tions without signs of infection at CT should be considered of US and fluoroscopy can improve on this by facilitating sterile until proven otherwise. Percutaneous drainage is safe needle puncture using US guidance followed by optimal generally avoided in this context due to the potential risk drain positioning using fluoroscopic guidance. of introducing infection. Deteriorating patients with high

Journal of Gastrointestinal and Abdominal Radiology ISGAR Vol. 3 No. 1/2020 Role of Interventional Radiology in the Management of Pancreatic Pathologies Salahia et al. 101 clinical suspicion of infection may benefit from US-guided aspiration to rule out an infected pancreatic necrosis. When infected necrosis is present, large-bore or multiple percuta- neous drainage catheters should be sited in the collection as a bridge or as an alternative to surgical debridement.12 Guidelines from 2013 by the International Association of Pancreatology and the American Pancreatic Association advise postponing all forms of invasive intervention in patients with infected necrosis, preferably until 4 weeks after the onset of disease.13 The rationale behind this is fourfold. First, antibiotics alone might be sufficient as treatment. Second, diagnosing infected necrotizing pan- creatitis is often easier in the later stages of the disease, when all other sources of infection or systemic inflamma- tory response have been ruled out. Third, catheter drain- age is typically easier once the collection has become Fig. 2 CT-guided guided drainage of peripancreatic collection through more liquefied and the stage of walled-off necrosis has a right posterior approach. been reached. Fourth, endoscopic transluminal drainage requires a walled-off collection. Pseudocyst Gastrostomy In theory, it is not always necessary to wait several weeks Iatrogenic communication between a pseudocyst and hollow until full encapsulation of peripancreatic collections and per- viscus can be formed to enable drainage (►Fig. 3). Internal cutaneous drainage can be performed safely and successfully gastric drainage of pancreatic pseudocysts is now commonly 14 in the first weeks after the onset of disease. If there is no performed under endoscopic US guidance.19 CT-guided per- technical reason for postponing catheter drainage, patients cutaneous technique cannot regularly provide an adequately with infected necrotizing pancreatitis might benefit from wide cystogastrostomy opening.11 Surgical cystogastrostomy earlier catheter drainage in terms of reducing the rate of is usually reserved for necrotic collections that do not abut complications and length of hospital stay. This is also the case the and may be found in the retroperi- in the context of abdominal compartment syndrome. More toneal space.19 recently, the Dutch Pancreatitis Study Group is undertaking a The percutaneous approach typically necessitates two randomized controlled trial (POINTER [postponed or imme- stages, with the pseudocyst initially being drained percuta- diate drainage of infected necrotizing pancreatitis]) that will neously through a transgastric route as a temporary bridge compare immediate and delayed catheter drainage in an before converting into an internal cystogastrostomy drain- attempt to further improve the outcome of these severely ill age through a double-J stent or by pushing the percutaneous 15 patients. drain into the .20 When a collection is located deep in the abdomen or is There is no consensus about the duration of drainage poorly visualized on US, computed tomography (CT) offers through pseudocyst gastrostomy. After the introduction of this adequate guidance to allow safe placement of percutaneous technique in 1984, pigtail catheter removal was initially advised 16 drains. after 3 months. The technique has since evolved such that the After placement and aspiration of fluid, self-locking pigtail catheter is left in situ for at least 1 year to more than 3 years if drains of size 8 to 12 Fr are left in place and irrigated with there is a concern that catheter removal would lead to symp- 10 to 20 mL of sterile saline three times daily. Catheters can tomatic recurrence. Catheter removal by forceps during routine be upsized to a maximum of 28 F, as the clinical situation gastroscopy in the outpatient setting has been reported.21 8 evolves if smaller drains prove inadequate. Technical success in percutaneous catheter placement External drainage of peripancreatic collections may fail in is greater than 90%, with an immediate complication rate the setting of abnormal pancreatic ductal anatomy. In a study of around 6% and a mortality rate of 1%.18 Secondary infec- by Nealon et al, there was a statistically significant difference tion with abscess formation is not uncommon, occurring in in successful percutaneous drainage between patients with around 11%.21 Complete resolution of the pseudocyst with normal pancreatic duct anatomy and those with a pancreatic this method has been reported in at least 88% of cases.18 duct stricture or duct disconnection.17 Drainage failed to per- manently resolve the collection in half of the patients with Treatment duct strictures and was uniformly unsuccessful in patients Pancreatic fistulas may complicate pancreatic surgery or nec- with ductal disconnection or occlusion. rotizing pancreatitis.22 They can communicate with bowel The incidence of cyst–cutaneous fistula formation is loops, , or other adjacent viscera.23 reportedly as high as 50% in certain settings18; therefore The incidence of gastrointestinal fistulation following internal transgastric drainage is preferable in situations in acute pancreatitis is reportedly 3 to 47%, with an associated which a persistent pseudocyst is being driven by a persisting increase in mortality of up to 34.7% in those with pancreatic pancreatic duct fistula (►Fig. 2). colonic fistulae.24

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Fig. 3 (A, B) Coronal and axial maximum intensity projection reformatted CT (computed tomography) showing pseudocyst gastrostomy.

In the presence of a fluid collection, percutaneous drain- peripancreatic fat, which, if loose, is extracted in a piecemeal age can treat the collection, and this may occasionally lead to fashion until, after several procedures, a cavity lined by viable spontaneous resolution of the fistula.16 If the main compo- granulation tissue is created. At the end of the procedure, an nent of a fistula is of biliary origin, transhepatic biliary drain 8-Fr catheter sutured to a 24-Fr drain is passed into the cavity insertion can lead to fistula closure by diverting bile from to allow continuous postoperative lavage of warm 0.9% nor- the site of the fistula. In cases with persisting biliary leak, mal saline.29 Chemically assisted debridement with hydrogen the placement of an occlusion balloon above the fistula may peroxide has been reported during endoscopic drainage.30 divert biliary flow away from the fistula.25 The necrotic pancreatic body and fatty tissue can also be

Direct fistula embolization has been found to be effective, fragmented using a snare catheter (LASSOS, Osypka Med- with access gained through the tract of a previous surgi- ical, Rheinfelden, Germany) and a Dormia basket advanced cal drain, through an image-guided percutaneous drain, or through the percutaneous sheath.27 Others described the use through a transhepatic approach. Once the fistula site has of a 14- to 16-Fr Malecot catheter (CR Bard Inc., Covington, been reached, different materials may be used to facilitate Georgia) for debridement by twisting it repeatedly inside the closure, including ethanol, particles, or glue.16,26 collection. An endoscopic clamp through an appropriately sized introducer sheath can also be used percutaneously for Percutaneous Necrosectomy the same purpose.31 Following liquefaction and encapsulation of necrotic pan- creatic tissue, persistent infection of these cavities despite Vascular Interventions percutaneous drainage has been ascribed to the formation and infection of sequestered solid necrotic tissue that is Endovascular Treatment of Bleeding presumed to be inaccessible to antibiotics.27 Surgical necro- Peripancreatic Pseudoaneurysm Embolization sectomy has historically been the mainstay of treatment for Pseudoaneurysms develop in approximately 4 to 8% of symptomatic patients.28 However, in the current era, when patients with chronic pancreatitis and less frequently in the percutaneous or endoscopic drainage of pancreatic abscess/ context of acute pancreatitis.32,33 They most commonly affect infected necrotic collection fails, there may be a role for per- the splenic artery followed by gastroduodenal, pancreati- cutaneous necrosectomy in patients who are not fit for open coduodenal, and hepatic arteries.34 or laparoscopic drainage.27 The etiology is attributed to an enzymatic insult to peri- The procedure is performed by exchanging a preexisting pancreatic arteries or erosion of a pseudocyst into adjacent left flank drain for a guidewire. Right-sided or transperito- visceral arteries. Although rupture of a pseudoaneurysm is neal drainage is also possible.29 A low-compliance balloon rare, it is a serious complication, potentially resulting in mas- dilator is inserted into the collection and dilated to up to 30 Fr. sive hemorrhage with concomitant significant clinical dete- Access to the cavity is achieved by passing a nephroscope (or rioration. A mortality rate of up to 37% has been reported.35 similar) through a sheath, which allows debridement under Early detection of pseudoaneurysms is important to direct vision. The nephroscope has an operating channel that prevent subsequent rupture and catastrophic outcomes permits standard (5 mm) laparoscopic graspers as well as an (►Fig. 4). Abdominopelvic CT is the imaging modality of irrigation/suction channel. High-flow lavage promotes initial choice in patients with complicated pancreatitis. Images evacuation of pus and liquefied necrotic material, exposing are obtained following intravenous administration of residual black or gray devascularized pancreatic necrosis and 100 to 150 mL of iodinated contrast material at a rate of

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Fig. 4 A 48-year-old man with a peripancreatic collection as a sequel of acute pancreatitis was treated with a percutaneous drain (yellow arrow). Follow-up CT (computed tomography) during his admission revealed a splenic artery pseudoaneurysm, which was overlooked at the time of scanning (blue arrow). A few days later, the pseudoaneurysm ruptured and the patient presented with massive fresh rectal hemor- rhage. As displayed in (B), The left flank drain has eroded its way into the descending colon, with side holes inside and outside the bowel.

3.5 mL/second or higher using a mechanical power injec- In a series of 37 patients with visceral artery pseudoaneu- tor. Craniocaudal pancreatic scanning is performed during rysms embolized with coils using the isolation technique, 32 breath-hold and commenced 30 to 50 seconds from the start patients had confirmed complete resolution of pseudoaneu- of the contrast injection (pancreatic parenchymal phase). rysms on CT scans obtained at 1 day postprocedure, although This imaging technique is suitable for the detection and two cases of recurrence were seen during follow-up.42 follow-up of nonvascular complications of pancreatitis, as Several recent studies have reported the effectiveness of well as venous and most arterial complications. Detection of transcatheter arterial embolization with N-butyl cyanoacry- more subtle arterial complications (small pseudoaneurysms late (NBCA) glue.43,44 According to Toyoda et al, the hemostasis and subtle arterial hemorrhage) may require confirmation ratios for acute gastroduodenal bleeding treated by tran- with CT angiography or catheter angiography in indetermi- scatheter arterial embolization with NBCA and transcathe- nate cases.36 ter arterial embolization with gelatin sponge particles and/ Several techniques for the endovascular treatment of or coils are 85.7 and 78.3%, respectively. When the isolation pseudoaneurysms have been reported in the literature technique cannot be performed, NBCA embolization is rec- using various embolization agents, such as embolization ommended as an alternative.40 of the aneurysm neck, embolization proximal to the pseu- Stent grafts can be used to exclude pseudoaneurysm if the doaneurysm, and embolization of vessels both distal and neck is unfavorable or when the parent artery is nonexpend- proximal to the pseudoaneurysm, the so-called “isolation” able (e.g., the superior mesenteric artery [SMA]).33 or “sandwich” technique.37-39 Preference for a specific ther- Bovine thrombin is also an option as an endovascular apeutic approach must take into consideration several fac- embolic agent. Although an off-label use of the thrombin, tors such as the anatomical location of the affected vessel, it has also been used for percutaneous direct puncture and the nature of the artery (expendable with extensive collat- embolization of pseudoaneurysm by injecting thrombin into eral circulation vs. nonexpendable), the size of pseudoan- the pseudoaneurysm as well as the surrounding fluid collec- eurysm sac, and the patient’s hemodynamic status.33 tion percutaneously under CT guidance.45,46 Although embolization of the aneurysmal neck can spare Other materials used for percutaneous direct puncture blood flow in the parent artery, infusion of the embolization for pancreatitis-related pseudoaneurysm treatment include material may induce rupture due to the fragility of the aneurysm glue,47 Gelfoam,43 PVA (polyvinyl alcohol) particles,48 and wall.40 In addition, this technique increases the risk of migration coils,48 with variable success rates. of embolic materials.41 Embolization at a point proximal to the If there is a concern that high-velocity blood flow will pseudoaneurysm is generally a more straightforward technique increase the risk of nontarget embolization when using liq- but carries a higher risk of failure secondary to blood flow from uid embolic agents and coils, vascular occlusion plugs may collateral vessels. It is for this reason that the isolation technique be useful, providing a well-controlled and stable occlusion. using aneurysm coils is considered the optimal endovascular Vascular occlusion plugs also have the advantage of having approach in patients with visceral artery pseudoaneurysms.42 a more flexible delivery system when compared with stent

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grafts, and recent advances in technology have seen the 19.5%, and severe capillary and venous bleeding associated introduction of plugs deliverable through a microcatheter.33 with pancreatic necrosis in 19.5%. Overall, transarterial embolization of pancreatitis-related It is not always possible to identify a single culprit vessel pseudoaneurysms is relatively safe and effective. Recurrence on CT or angiography; hence, surgical treatment is suggested or new pseudoaneurysm formation rates are low and usually in case of severe venous or diffuse capillary bleeding, hemor- occur within 6 months of embolization.49 rhagic pseudocysts, and unsuccessful embolization (►Fig. 6). Venous pseudoaneurysms are an extremely rare compli- cation of pancreatitis, with a handful of known cases follow- Pancreatic Arteriovenous Malformation Embolization ing pancreatic surgery or abdominal trauma.50,51 Spontaneous Pancreatic AVM (P-AVM) is rare (~90 cases have been resolution has been reported, with a natural progression reported).58 They may be congenital in association with hered- to thrombosis. In another case, a posttraumatic superior itary hemorrhagic telangiectasia or Osler–Weber–Rendu’s mesenteric vein pseudoaneurysm was treated with coiling disease. They may also be posttraumatic or occur following through a percutaneous transhepatic approach.51 pancreatic transplantation, neoplasm, or inflammation.59 The majority of patients with P-AVM remain asymptom- Ruptured Pseudoaneurysm into a Pseudocyst atic. Gastrointestinal hemorrhage may occur from a ruptured (Hemosuccus Pancreaticus) varix secondary to or direct erosion of A peripancreatic pseudoaneurysm may rarely rupture into a the AVM into the pancreatic/ or through the adja- pancreatic pseudocyst, with hemorrhage traveling through cent intestinal mucosa as a duodenal ulcer.58 the pancreatic duct into the gastrointestinal tract through The pancreatic head is most commonly involved (56%) the ampulla of Vater (►Fig. 5). This condition, “hemosuccus followed by the body and tail (33%), with the entire pan- pancreaticus” (HP), was first reported by Sandblom in 1970, creas involved in 7%. The definitive treatment for P-AVM with an estimated incidence of 1 in 1,500 cases of acute gas- has traditionally been surgical resection.60 However, Bruno trointestinal hemorrhage.52 et al described a case of a P-AVM communicating the splenic The most common cause of HP is chronic recurrent pan- artery, the superior pancreatic artery, and the splenic vein.61 creatitis related to chronic alcoholism, which results in pan- This was treated with coil embolization of the two feeding creatic pseudocyst formation.53 The peripancreatic vessels arteries, with no significant filling of the portal vein on sub- most commonly involved are splenic, gastroduodenal, pan- sequent angiography. creaticoduodenal, gastric, and hepatic arteries.54

The most common symptoms are melena and upper Oncological Interventions abdominal pain. Visualization of spurting blood from the ampulla of Vater is diagnostic.55 However, because of the Percutaneous Biopsy typically intermittent nature of the bleeding, and difficulty Biopsy can be performed intraoperatively, endoscopically, visualizing bleeding from the ampulla of Vater using an or percutaneously with CT or US guidance.62 Percutaneous end-viewing endoscope, upper gastrointestinal imaging-guided fine needle aspiration (FNA) has been in use establishes the diagnosis in only 30% of cases.56 Diagnosis can since the 1970s, but it can be challenging to establish a defin- often be challenging with only a suspicion of a pseudoaneu- itive diagnosis of pancreatic adenocarcinoma from cytol- rysm on cross-sectional imaging. Treatment approach is sim- ogy samples. As an alternative, image-guided percutaneous ilar to other peripancreatic pseudoaneurysms. biopsy of the pancreas with an automated core biopsy needle has become more commonly used.63 Hemorrhagic Pseudocysts A retrospective study by Yang et al reviewed a sampling As previously described, pseudoaneurysms can be of 88 pancreatic masses: 13 underwent FNA only, 60 under- free-standing or can be located within a pseudocyst. Further- went core needle biopsy only, and 15 underwent both.64 more, pseudocysts can erode into an adjacent artery, forming The diagnostic accuracy of core biopsy alone and both core an expanding hemorrhagic cyst that can rupture into an adja- biopsy and FNA was comparable at 93.3% and was margin- cent hollow organ, or can communicate with the pancreatic ally lower for patients who underwent FNA alone (92.3%). duct producing HP.32 The negative predictive value was 57% overall for all biop- The overall incidence of bleeding associated with pan- sies. This is too low for a reliable exclusion of the presence of creatitis is not well established. The prevalence of bleeding pancreatic malignancy and suggests that negative results of pseudocysts ranges from 2 to 31%.32,57 While most life-threat- percutaneous biopsy, whether core or FNA, should be viewed ening hemorrhage is arterial in origin, venous bleeding can with caution. occur, as well as massive diffuse small vessel hemorrhage associated with pancreatic necrosis. Percutaneous Transhepatic Biliary Drainage Spontaneous abdominal hemorrhage can develop at Malignant biliary obstruction is most commonly associ- any time in patients with a history of pancreatitis but is ated with pancreatic carcinoma, developing in 70 to 90% of often a late complication, with a mean time of occurrence patients and typically leading to jaundice, pruritus, hepa- of 2.3 years.32 In Balthazar and Fisher’s series of 16 patients tocellular dysfunction, malabsorption coagulopathy, and with pancreatitis-related hemorrhage, bleeding was second- cholangitis.65 Biliary decompression may be achieved by ary to pseudoaneurysms in 61%, hemorrhagic pseudocysts in endoscopic retrograde cholangiopancreatography (ERCP)

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Fig. 5 Coronal reformatted CT (computed tomography) in (A) arterial and (B) portal venous phases in an 89-year-old male patient with mas- sive upper gastrointestinal (GI) hemorrhage. There is evidence of rupture of splenic artery pseudoaneurysm (yellow arrow) into a pancreatic tail pseudocyst (blue arrows). The GI hemorrhage was presumed to be coming from a pseudocyst eroding through the stomach (green arrow). (C, D) This was treated successfully with coil embolization of the splenic artery.

Fig. 6 A 28-year-old male with previous gallstone pancreatitis underwent a follow-up MRI (magnetic resonance imaging) for a known pseudo- cyst. (A) Coronal FIESTA (fast imaging employing steady-state acquisition) sequence demonstrates isointense material within pancreatic pseudocyst suspicious of hemorrhage. (B) Arterial phase coronal CT (computed tomography) shows high-density material within the cyst in keeping with hemorrhage; however, no pseudoaneurysm was seen. The patient underwent catheter angiography, which did not reveal a site of active contrast extravasation or a pseudoaneurysm (not shown).

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or through percutaneous transhepatic biliary drainage Mortality attributed to percutaneous biliary tract interven- (PTBD). tions alone is much rarer and ranges from 0.1 to 0.8%.69 Endoscopic insertion of plastic or metal stents is technically successful in approximately 90 to 95% of malignant biliary Ablative Therapies obstruction cases.66 If ERCP fails due to inaccessible papilla due Experience and data with pancreatic tumor ablative therapy to congenital or surgically altered anatomy, failed cannulation, are regarded as investigational and limited.4 Brachytherapy or the presence of severe tumor-induced stricturing of the bile delivered by a percutaneous approach has been found to duct and/or duodenum, PTBD can be undertaken4 (►Fig. 7). be minimally effective. Other endoscopic ablative therapies An intrahepatic bile duct branch is accessed (under fluo- have been trialed, including endoscopic fiducial markers and roscopic and/or US guidance) with an 18- to 22-gauge nee- brachytherapy, photodynamic therapy, EUS-guided radiof- dle followed by a 0.018-inch guidewire. Puncture with a requency ablation (RFA), and EUS-guided alcohol ablation.4 smaller caliber (22-gauge) needle has been shown to be safer We will focus on other nonendoscopic percutaneous inter- in patients without intrahepatic bile duct dilatation.4 Intra- ventions including percutaneous RFA, microwave ablation, ductal position is confirmed by a backflow of bile or by flu- irreversible electroporation (IRE), and electrochemotherapy oroscopic visualization of injected contrast. The 0.018-inch (ECT). Their current role in the treatment of pancreatic can- guidewire is exchanged for a 0.035-inch guidewire. Depend- cer is still under investigation. ing on operator preference, an access sheath (generally 6 Fr or larger) may be used and the stricture crossed using a cath- Radiofrequency Ablation eter and guidewire. After crossing the stricture, the wire is Wu et al first described open surgical RFA for unresectable exchanged for a stiff wire. The drainage catheter or stent is pancreatic tumors.70 Sixteen patients with unresectable pan- then deployed. Internal/external drains must have side holes creatic cancer were treated by open cool-tip RFA, a with high on each side of the obstruction but not extending into the mortality rate (25%) due to dramatic direct portal venous liver parenchyma as this leads to bile leak. Stents must com- gastrointestinal hemorrhage and acute renal failure. pletely cover the lesion. In a later study by Girelli et al, 50 patients with locally Drainage is successful in approximately 95% of patients advanced pancreatic cancer underwent US-guided RFA with dilated intrahepatic bile ducts but only 70% of during .71 RFA was the only treatment in 19 patients with nondilated ducts.67 patients. RFA was combined with biliary and gastric bypass Results from a national audit of 833 patients in the United in 19 patients, gastric bypass alone in 8, biliary bypass alone

Kingdom who had undergone PTBD in 2009 showed high in 3, and pancreaticojejunostomy in 1. There was only one immediate technical success for drainage and stenting (>95%). case of 30-day mortality in this series. The reported RFA- Minor complications occurred in 26.0% of patients, the most related complications were two cases of pancreatic fistulas common being pain (14.3%), sepsis (7.7%), and hemorrhage and four cases of portal vein thrombosis.71 (4.5%). Major complications occurred in 7.9% of patients, the most common being hemorrhage (3.5%), renal failure (1.8%), Microwave Ablation and sepsis (1.6%).68 Data also showed a high inhospital mor- High-frequency (2.45-GHz) microwave ablation (MWA) for tality rate (19.8%) in patients with malignancy. However, this the treatment of unresectable and nonmetastatic locally high mortality cannot be entirely attributable to the proce- advanced pancreatic cancer has been trialed by Lygidakis dure and is considered to most likely reflect the underlying et al.72 It has been suggested as a local effective procedure disease and multiple comorbidities in this patient group.68 that is feasible and safe, with acceptable minor complications

Fig. 7 (A) Coronal reformatted CT (computed tomography) demonstrates pancreatic head tumor (yellow arrow) causing biliary tree dilatation (blue arrow). (B) This was treated with percutaneous transhepatic biliary drainage.

Journal of Gastrointestinal and Abdominal Radiology ISGAR Vol. 3 No. 1/2020 Role of Interventional Radiology in the Management of Pancreatic Pathologies Salahia et al. 107 in locally advanced pancreatic tumors, which can be used as The pancreatic exocrine enzymes can be drained directly part of a palliative or multimodality treatment. into the enteric circulation by constructing a side-to-side However, the feasibility and safety of percutaneous MWA anastomosis between the donor duodenum and the recipient approach require further evaluation.72 small bowel or recipient bladder (►Fig. 8).

Percutaneous Irreversible Electroporation Vascular Complications of the Transplanted Pancreas This is a nonthermal ablative technology first described in Vascular complications of the transplanted pancreas can 2009 by Garcia et al.73 It uses high-voltage low-energy direct be broadly divided into thrombosis, stenosis, hemorrhage, current through electrodes placed into the pancreas percuta- aneurysms, and AVM.77,78 neously under CT guidance to create permanent pores in the Imaging investigations usually start with a Doppler study cell membrane, leading to cell death. to determine the presence of waveform tracings from the The largest retrospective review of patients with pan- implicated vessel. Suspicious duplex US findings should be creatic adenocarcinoma who underwent percutaneous IRE evaluated with contrast-enhanced CT or contrast-enhanced was conducted at Miami Cancer Institute in 2014.74 The magnetic resonance imaging (MRI); these noninvasive modal- study included 50 patients with biopsy-proven unresectable ities have largely replaced catheter angiography as means of pancreatic cancer. The overall survival for the entire cohort diagnosis, although the latter remains the gold standard for from the date of IRE was 14.5 months (95% confidence inter- the assessment of pancreatic artery complications following val: 10.4–18.6 months). Complications occurred in 20% of transplant.78 One advantage of catheter angiography is the patients, including pancreatitis, pain, sepsis, and gastric leak. ability to proceed directly to endovascular treatment in the same procedure. Electrochemotherapy ECT is an electroporation-based therapy with an already Transplant Artery Thrombosis established place in the treatment of cutaneous and liver This is the most severe posttransplantation vascular compli- tumors. cation predisposing the graft to dysfunction and necrosis.1 It Only one case series (clinical phase I/II) of intraoperative most commonly occurs within the first 3 months following pancreatic ECT with 13 patients has been reported.75 Intraop- transplantation. erative electrodes were inserted with US guidance into and The symptoms of thrombosis include unexplained hyper- around the tumor followed by an intravenous bolus of bleo- glycemia, tenderness over the graft, graft enlargement, and, mycin (15,000 IU/m2) and subsequent electric pulses by an in bladder-drained grafts, hematuria and decreased urinary electric pulse generator. Treatment was completed within the amylase.6 time window of 8 to 28 minutes after the end of the bleomy- Accurate and expedient imaging diagnosis of arterial cin bolus. This time window ensured the maximum concen- thrombosis is essential because early revascularization tration of drug within the lesion. No intra- or postoperative serious adverse events related to ECT were observed.75 Further research is being undertaken to evaluate the safety and efficacy of this technique in pancreatic cancer treatment.76

Interventional Radiology for the Transplanted Pancreas

Pancreas transplantation is most frequently performed in conjunction with kidney transplantation in the cases of end-stage renal failure secondary to type 1 diabetes. This procedure is known as simultaneous pancreas–kidney transplantation.1 The pancreas allograft and a short segment of duodenum are typically placed intraperitoneally in the right side of the abdomen, with the donor kidney generally placed in the left iliac fossa. A donor iliac artery Y-conduit is anastomo- sed between the SMA and splenic artery of the graft and the common or external iliac artery of the recipient. The venous outflow of the pancreas graft may be drained either system- Fig. 8 Simultaneous pancreas–kidney transplantation. Yellow arrow ically into the recipient inferior vena cava or by end-to-side indicates transplant artery graft, blue arrow indicates transplant vein anastomosis from the donor portal vein to the recipient com- graft, and green arrow indicates duodenojejunal anastomosis. PV, mon or external iliac vein. portal vein; Tx K, transplanted kidney; Tx. P, transplanted pancreas.

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with or without thrombectomy may salvage the graft79 Pancreatic Transplant Vein Thrombosis (►Figs. 9 and 10). Venous thrombosis is the most common cause of early tech- Predisposing factors include prolonged cold ischemia, nical pancreatic transplant failure (70%).82 Early thrombosis prolonged back-table preparation, graft rejection, pancreati- may be associated with acute or hyperacute rejection. How- tis, stump thrombi, and vessel trauma.79 ever, the majority (60%) of grafts lost to thrombosis are histo- Complications of pancreas graft thrombosis include graft pathologically normal. dysfunction, leakage of pancreatic secretions, pancreatitis, The etiology is thought to be due to relative stasis caused necrosis, and sepsis. Prompt surgical exploration is often by compression by a perianastomotic fluid collection, due required.6 to phlebitis related to pancreatitis, or because of the shift in organ position, leading to stretching or twisting of the 83 Transplant Artery Stenosis venous anastomosis. Given that pancreas grafts are predisposed to thrombo- Arterial stenosis following pancreas transplantation is less sis, some propose routine postoperative anticoagulation.84 common than arterial thrombosis and is typically an early Meticulous surgical technique and rigorous avoidance of posttransplantation complication.1 Predisposing factors the transplant organ damage are considered to be more include rejection clamp injury, faulty surgical technique, effective methods to decrease the incidence of early catheter-induced trauma, and disruption of the vasa vaso- thrombosis.85 rum.80 This is usually assessed with arterial Doppler, with Endovascular treatments of pancreas transplant venous a peak systolic velocity of 2 m/second or greater being sug- thrombosis include thrombolysis, mechanical thrombec- gestive of an arterial stenosis greater than 50%.1 tomy, and deployment of metal stents for anastomotic steno- Treatment options for arterial stenosis include angioplasty, sis or kinks (►Fig. 13).85 covered stent placement in selected cases, and surgical revas- cularization.81 Early treatment with revascularization preserves Pancreatic Transplant Arteriovenous Fistula graft function and often prevents retransplantation (►Fig. 11). Embolization An arteriovenous fistula (AVF) is most commonly the conse- Pancreatic Transplant Hemorrhage quence of biopsy of the transplanted allograft when the walls Intra-abdominal bleeding in the early period after pan- of both artery and vein are iatrogenically lacerated.1 It, how- creas transplantation is typically associated with systemic ever, can be iatrogenic soon after pancreatic transplantation, 6 anticoagulation initiated to prevent graft thrombosis. as in our case (►Fig. 14). However, delayed hemorrhage is typically secondary to At duplex US, an AVF is identified as a focal area of aliasing pseudoaneurysm rupture. involving a high-velocity low-resistance feeding artery and In common with treatment of other visceral pseudoaneu- a pulsatile “arterialized” draining vein.86 Dual-phase (arterial rysms, endovascular embolization is usually the first line of and portal venous) CT helps in the characterization and ana- therapy, offering better morbidity and mortality than open tomical localization of these vessels. surgical interventions. A covered stent can be deployed in the AVFs may be associated with regional areas of transient common/external iliac artery to exclude the pseudoaneu- parenchymal enhancement on contrast-enhanced CT/MRI. rysm (►Fig. 12). Surgical exploration may be necessary when Large AVFs may cause graft ischemia and dysfunction due to endovascular treatment fails or where hematoma evacuation arterial “steal” phenomenon.1 They are usually treated with is required.6 transarterial embolization.

Fig. 9 Blue arrows point to the site of the proximal occlusion of the upper of the two transplanted pancreas arteries on (A) coronal maximum intensity projection reformatted CT (computed tomography) and (B) digital subtraction angiography. Revascularization (yellow arrow) was achieved using 2-mm balloon angioplasty.

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Fig. 10 A 26-year-old female who underwent pancreatic transplantation 4 months previously presented with a firm mass in the right iliac fossa. (A) Computed tomographic angiography (B) digital subtraction angiography show right external iliac artery (EIA) occlusion (green arrow) shortly after Y graft. EIA reforms at the level of the inguinal ligament (yellow arrow). Note that the pancreatic transplant arterial anastomosis is widely patent, and so are both branches (blue arrows). This was treated with a prosthetic vascular graft (not shown).

Fig. 11 A 31-year-old male who underwent pancreatic and kidney transplant 4 years previously was admitted with urinary tract infection, sepsis, and right iliac fossa pain. (A) Coronal maximum intensity projection reformatted CT (computed tomography) shows occluded Y graft (green arrow) and no enhancement of the pancreas. (B, C) The patient underwent angioplasty and stent deployment.

Nonvascular Interventions on the Transplanted Pancreas No major complications occurred in a series of Due to the lack of consistent clinical symptoms or markers for 42 attempted percutaneous biopsies.87 However, there is a rejection, pancreatic biopsies have become the standard method risk of causing vascular damage to the allograft, including in diagnosing transplant rejection. The biopsy techniques are AV fistulation.1 either through cystoscopy or by percutaneously using US and/or Similar to native pancreas percutaneous interventions, CT guidance, with a reported success rate of 83%.87 Cystoscopic drainage of peripancreatic transplant collections can be biopsies require general anesthesia and only allows biopsy of attempted on the transplanted pancreas with US or CT the pancreatic head.88 guidance.

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Fig. 12 A 38-year-old female with a previously failed pancreatic transplantation presented with acute hematuria and deranged clotting. (A) Abdominal CT (computed tomography) suggests active hemorrhage (yellow arrow) from the right common iliac artery (CIA) into the bladder through the trans- planted pancreas’ duodenal pouch (green arrow). (B) Angiography confirms right CIA contrast extravasation. (C) This was treated with a covered stent.

Fig. 13 A 35-year-old female presented with severe hyperglycemia at day 5 following simultaneous pancreas–kidney transplantation. (A) Coronal oblique maximum intensity projection reformatted CT (computed tomography) shows a filling defect within the vein graft in keeping with nonocclusive thrombus (blue arrow). (B) Catheter venography confirms graft thrombus (yellow arrow). (C) This was treated with mechanical thrombectomy.

Fig. 14 (A) Axial CT (computed tomography) demonstrates an arteriovenous fistula (AVF) in the transplanted pancreas (yellow arrow). (B) Three-dimensional reconstruction of the AVF. IVC, inferior vena cava.

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Conclusion 13 Working Group IAP/APA Acute Pancreatitis Guidelines. IAP/ APA evidence-based guidelines for the management of acute The anatomical location of the pancreas has meant that his- pancreatitis. Pancreatology 2013;13(4, Suppl 2):e1–e15 torically, pancreatic pathologies were treated by either major 14 van Grinsven J, van Santvoort HC, Boermeester MA, et al. surgery or conservative means. Dutch Pancreatitis Study Group. Timing of catheter drainage in infected necrotizing pancreatitis. Nat Rev Gastroenterol Hepa- Image-guided percutaneous intervention for a wide range tol 2016;13(5):306–312 of pancreatic disease is now routine. 15 van Grinsven J, van Dijk SM, Dijkgraaf MG, et al. Dutch Pan- Vascular complications of pancreatic disease benefit from creatitis Study Group. Postponed or immediate drainage of accurate diagnosis with modern imaging techniques and may infected necrotizing pancreatitis (POINTER trial): study proto- require immediate treatment. Endovascular intervention for col for a randomized controlled trial. Trials 2019;20(1):239 the treatment of arterial and venous peripancreatic pathol- 16 Mauri G, Mattiuz C, Sconfienza LM, et al. Role of interven- tional radiology in the management of complications after ogy is demonstrably effective. pancreatic surgery: a pictorial review. Insights Imaging Ablative techniques from cancer are emerging and may 2015;6(2):231–239 help to alleviate the high morbidity and mortality associated 17 Nealon WH, Bhutani M, Riall TS, Raju G, Ozkan O, Neilan R. with pancreatic cancer and its treatment. A unifying concept: pancreatic ductal anatomy both predicts Vascular complications of the transplanted pancreas can and determines the major complications resulting from pan- creatitis. J Am Coll Surg 2009;208(5):790–799 be severe and cause early technical pancreatic transplanta- 18 Swartz DK, Obando J. Endoscopic management of peri-pancre- tion failure. Percutaneous pancreas transplant biopsy has a atic collections. Gastroenterol Res Pract 2012;2012:906381 high success rate and is most accurate in diagnosing trans- 19 Shamah S, Okolo PI III. Systematic review of endoscopic­ plant rejection. Advances of endovascular interventions per- cyst gastrostomy. Gastrointest Endosc Clin N Am 2018; mit revascularization and may salvage the graft. 28(4):477–492 20 Khreiss M, Zenati M, Clifford A, et al. Cyst gastrostomy and Conflict of Interest necrosectomy for the management of sterile walled-off pan- None declared. creatic necrosis: a comparison of minimally invasive surgical and endoscopic outcomes at a high-volume pancreatic center. J Gastrointest Surg 2015;19(8):1441–1448 References 21 Henriksen FW, Hancke S. Percutaneous cystogastros- tomy for chronic pancreatic pseudocyst. Br J Surg 1 Low G, Crockett AM, Leung K, et al. Imaging of vascular com- 1994;81(10):1525–1528 plications and their consequences following transplantation in 22 Hackert T, Werner J, Büchler MW. Postoperative pancreatic fis-

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